Neocortical dendritic complexity is controlled during development by NOMA-GAP-dependent inhibition of Cdc42 and activation of cofilin

Genes and Development

Volumn 26, Issue 15, 2012, Pages 1743-1757

  Rosário, Marta ^a,b   Schuster, Steffen ^a   Jüttner, René ^c   Parthasarathy, Srinivas ^a   Tarabykin, Victor ^a   Birchmeier, Walter ^b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b Department of Signal Transduction Invasion and Metastasis of Epithelial Cells ^*  (Germany)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Cdc42; Cofilin; Dendritic branching; Dendritic complexity; Neocortical development; Neuronal differentiation; NOMA GAP

Indexed keywords

COFILIN; GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; LIM KINASE 1; PROTEIN CDC42; PROTEIN LIMK2; PROTEIN NOMA GAP; PROTEIN PAK; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TUBULIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUDITORY CORTEX; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN REGION; BRAIN SIZE; CONTROLLED STUDY; DENDRITE; DEVELOPMENTAL STAGE; EMBRYO; ENZYME ACTIVATION; ENZYME MECHANISM; ENZYME REPRESSION; FEMALE; IN VIVO STUDY; MITOSIS; MOUSE; NEOCORTEX; NONHUMAN; PARIETAL CORTEX; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SOMATOSENSORY CORTEX;

ACTIN DEPOLYMERIZING FACTORS; ANIMALS; CDC42 GTP-BINDING PROTEIN; CELLS, CULTURED; DENDRITES; FEMALE; GTPASE-ACTIVATING PROTEINS; MICE; MICE, TRANSGENIC; NEOCORTEX;

ANIMALIA; MUS;

EID: 84864771989     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.191593.112     Document Type: Article

References (55)

1. Aizawa H, Wakatsuki S, Ishii A, Moriyama K, Sasaki Y, Ohashi K, Sekine-Aizawa Y, Sehara-Fujisawa A, Mizuno K, Goshima Y, et al. 2001. Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse. Nat Neurosci 4: 367-373.
2. Arber S, Barbayannis FA, Hanser H, Schneider C, Stanyon CA, Bernard O, Caroni P. 1998. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393: 805-809.
3. Armstrong DD, Dunn K, Antalffy B. 1998. Decreased dendritic branching in frontal, motor and limbic cortex in Rett syndrome compared with trisomy 21. J Neuropathol Exp Neurol 57: 1013-1017.
4. Bauman ML, Kemper TL, Arin DM. 1995. Pervasive neuroana-tomic abnormalities of the brain in three cases of Rett's syndrome. Neurology 45: 1581-1586.
5. Bellenchi GC, Gurniak CB, Perlas E, Middei S, Ammassari-Teule M, Witke W. 2007. N-cofilin is associated with neuronal migration disorders and cell cycle control in the cerebral cortex. Genes Dev 21: 2347-2357.
6. Bernstein BW, Bamburg JR. 2010. ADF/cofilin: A functional node in cell biology. Trends Cell Biol 20: 187-195.
7. Britanova O, de Juan Romero C, Cheung A, Kwan KY, Schwark M, Gyorgy A, Vogel T, Akopov S, Mitkovski M, Agoston D, et al. 2008. Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 57: 378-392.
8. Cappello S, Attardo A, Wu X, Iwasato T, Itohara S, Wilsch-Brauninger M, Eilken HM, Rieger MA, Schroeder TT, Huttner WB, et al. 2006. The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat Neurosci 9: 1099-1107.
9. Chai X, Forster E, Zhao S, Bock HH, Frotscher M. 2009. Reelin stabilizes the actin cytoskeleton of neuronal processes by inducing n-cofilin phosphorylation at serine3. J Neurosci 29: 288-299.
10. Chen TJ, Gehler S, Shaw AE, Bamburg JR, Letourneau PC. 2006. Cdc42 participates in the regulation of ADF/cofilin and retinal growth cone filopodia by brain derived neurotrophic factor. J Neurobiol 66: 103-114.
11. Coleman PD, Riesen AH. 1968. Environmental effects on cortical dendritic fields. I. Rearing in the dark. J Anat 102: 363-374.
12. Dan C, Kelly A, Bernard O, Minden A. 2001. Cytoskeletal changes regulated by the PAK4 serine/threonine kinase are mediated by LIM kinase 1 and cofilin. J Biol Chem 276: 32115-32121.
13. de Anda FC, Meletis K, Ge X, Rei D, Tsai LH. 2010. Centrosome motility is essential for initial axon formation in the neo-cortex. J Neurosci 30: 10391-10406.
14. Edwards DC, Sanders LC, Bokoch GM, Gill GN. 1999. Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat Cell Biol 1: 253-259.
15. Etienne-Manneville S, Hall A. 2002. Rho GTPases in cell biology. Nature 420: 629-635.
16. Gao FB, Brenman JE, Jan LY, Jan YN. 1999. Genes regulating dendritic outgrowth, branching, and routing in Drosophila. Genes Dev 13: 2549-2561.
17. Garvalov BK, Flynn KC, Neukirchen D, Meyn L, Teusch N, Wu X, Brakebusch C, Bamburg JR, Bradke F. 2007. Cdc42 regulates cofilin during the establishment of neuronal polarity. J Neurosci 27: 13117-13129.
18. Goebbels S, Bormuth I, Bode U, Hermanson O, Schwab MH, Nave KA. 2006. Genetic targeting of principal neurons in neocortex and hippocampus of NEX-Cre mice. Genesis 44: 611-621.
19. Hall A, Lalli G. 2010. Rho and Ras GTPases in axon growth, guidance, and branching. Cold Spring Harb Perspect Biol 2: a001818. doi: 10.1101/cshperspect.a001818.
20. Huttenlocher PR. 1974. Dendritic development in neocortex of children with mental defect and infantile spasms. Neurology 24: 203-210.
21. Irie F, Yamaguchi Y. 2002. EphB receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP. Nat Neurosci 5: 1117-1118.
22. Jan YN, Jan LY. 2010. Branching out: Mechanisms of dendritic arborization. Nat Rev Neurosci 11: 316-328.
23. Judas M, Sedmak G, Rados M, Sarnavka V, Fumic K, Willer T, Gross C, Hehr U, Strahl S, Cuk M, et al. 2009. POMT1-associated Walker-Warburg syndrome: A disorder of dendritic development of neocortical neurons. Neuropediatrics 40: 6-14.
24. Kaufmann WE, Moser HW. 2000. Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 10: 981-991.
25. Kurokawa K, Itoh RE, Yoshizaki H, Nakamura YO, Matsuda M. 2004. Coactivation of Rac1 and Cdc42 at lamellipodia and membrane ruffles induced by epidermal growth factor. Mol Biol Cell 15: 1003-1010.
26. Lee A, Li W, Xu K, Bogert BA, Su K, Gao FB. 2003. Control of dendritic development by the Drosophila fragile X-related gene involves the small GTPase Rac1. Development 130: 5543-5552.
27. Li Z, Van Aelst L, Cline HT. 2000. Rho GTPases regulate distinct aspects of dendritic arbor growth in Xenopus central neurons in vivo. Nat Neurosci 3: 217-225.
28. Marin-Padilla M. 1972. Structural abnormalities of the cerebral cortex in human chromosomal aberrations: A Golgi study. Brain Res 44: 625-629.
29. McAllister AK, Katz LC, Lo DC. 1997. Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron 18: 767-778.
30. Meng Y, Takahashi H, Meng J, Zhang Y, Lu G, Asrar S, Nakamura T, Jia Z. 2004. Regulation of ADF/cofilin phos-phorylation and synaptic function by LIM-kinase. Neuro-pharmacology 47: 746-754.
31. Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD. 2007. Neuro-nal subtype specification in the cerebral cortex. Nat Rev Neurosci 8: 427-437.
32. Moriyama K, Iida K, Yahara I. 1996. Phosphorylation of Ser-3 of cofilin regulates its essential function on actin. Genes Cells 1: 73-86.
33. Newey SE, Velamoor V, Govek EE, Van Aelst L. 2005. Rho GTPases, dendritic structure, and mental retardation. J Neurobiol 64: 58-74.
34. Nobes CD, Hall A. 1995. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81: 53-62.
35. Ohta Y, Nishida E, Sakai H, Miyamoto E. 1989. Dephosphory-lation of cofilin accompanies heat shock-induced nuclear accumulation of cofilin. J Biol Chem 264: 16143-16148.
36. Parrish JZ, Kim MD, Jan LY, Jan YN. 2006. Genome-wide analyses identify transcription factors required for proper morphogenesis of Drosophila sensory neuron dendrites. Genes Dev 20: 820-835.
37. Price LS, Leng J, Schwartz MA, Bokoch GM. 1998. Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol Biol Cell 9: 1863-1871.
38. Redmond L, Kashani AH, Ghosh A. 2002. Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 34: 999-1010.
39. Rosario M, Franke R, Bednarski C, Birchmeier W. 2007. The neurite outgrowth multiadaptor RhoGAP, NOMA-GAP, regulates neurite extension through SHP2 and Cdc42. J Cell Biol 178: 503-516.
40. Rosso SB, Sussman D, Wynshaw-Boris A, Salinas PC. 2005. Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat Neurosci 8: 34-42.
41. Ruchhoeft ML, Ohnuma S, McNeill L, Holt CE, Harris WA. 1999. The neuronal architecture of Xenopus retinal ganglion cells is sculpted by rho-family GTPases in vivo. J Neurosci 19: 8454-8463.
42. Saito T. 2006. In vivo electroporation in the embryonic mouse central nervous system. Nat Protoc 1: 1552-1558.
43. Schule B, Armstrong DD, Vogel H, Oviedo A, Francke U. 2008. Severe congenital encephalopathy caused by MECP2 null mutations in males: Central hypoxia and reduced neuronal dendritic structure. Clin Genet 74: 116-126.
44. Schwamborn JC, Puschel AW. 2004. The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat Neurosci 7: 923-929.
45. Scott EK, Reuter JE, Luo L. 2003. Small GTPase Cdc42 is required for multiple aspects of dendritic morphogenesis. J Neurosci 23: 3118-3123.
46. Shaw P, Lerch J, Greenstein D, Sharp W, Clasen L, Evans A, Giedd J, Castellanos FX, Rapoport J. 2006. Longitudinal mapping of cortical thickness and clinical outcome in children and adolescents with attention-deficit/hyperactivity disorder. Arch Gen Psychiatry 63: 540-549.
47. Shi Y, Pontrello CG, DeFea KA, Reichardt LF, Ethell IM. 2009. Focal adhesion kinase acts downstream of EphB receptors to maintain mature dendritic spines by regulating cofilin activity. J Neurosci 29: 8129-8142.
48. Sholl DA. 1953. Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87: 387-406.
49. Sumi T, Matsumoto K, Takai Y, Nakamura T. 1999. Cofilin phosphorylation and actin cytoskeletal dynamics regulated by rho- and Cdc42-activated LIM-kinase 2. J Cell Biol 147: 1519-1532.
50. Sumi T, Matsumoto K, Shibuya A, Nakamura T. 2001. Activation of LIM kinases by myotonic dystrophy kinase-related Cdc42-binding kinase a. J Biol Chem 276: 23092-23096.
51. Takashima S, Ieshima A, Nakamura H, Becker LE. 1989. Dendrites, dementia and the Down syndrome. Brain Dev 11: 131-133.
52. Threadgill R, Bobb K, Ghosh A. 1997. Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42. Neuron 19: 625-634.
53. Wallace GL, Dankner N, Kenworthy L, Giedd JN, Martin A. 2010. Age-related temporal and parietal cortical thinning in autism spectrum disorders. Brain 133: 3745-3754.
54. Yang N, Higuchi O, Ohashi K, Nagata K, Wada A, Kangawa K, Nishida E, Mizuno K. 1998. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393: 809-812.
55. Yoo Y, Ho HJ, Wang C, Guan JL. 2009. Tyrosine phosphorylation of cofilin at Y68 by v-Src leads to its degradation through ubiquitin-proteasome pathway. Oncogene 29: 263-272.